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n engl j med 369;26 nejm.org december 26, 20132474

Medicare has options for alle-viating the shifting of resources away from hospitals serving more disadvantaged patients. First, the payment criteria in HVBP could be altered to give more weight to quality improvement than to qual-ity achievement. Second, instead of having all acute care hospitals compete against each other, Medi-care could create homogeneous competition pools, defined by re-gion, DSH index, hospital size, or other criteria. Hospitals could then compete only against other hospi-tals in the same competition pool. In that case, HVBP would be bud-get-neutral within each competi-tion pool, guaranteeing that cer-tain types of hospitals would not be systematically disadvantaged by the program. These two strate-gies can be criticized because they excuse poorer performance for hospitals with more disadvantaged patients, in effect reinforcing ex-

isting disparities in care. This critique must be weighed against the potential harm to vulnerable patients if certain classes of hos-pitals face resource reductions under the current system. Third, Medicare could increase the tech-nical assistance provided to hos-pitals with more disadvantaged patients, perhaps by directing Quality Improvement Organiza-tions to focus attention on hospi-tals with a high DSH index value.

Programs that tie financial in-centives to quality and efficiency have the potential to push our health care system to reward val-ue rather than volume. However, a redistribution of resources away from hospitals serving high num-bers of disadvantaged patients could increase disparities in care. Going forward, these programs must be carefully monitored and, if necessary, modified to avoid such unintended consequences.

Disclosure forms provided by the author are available with the full text of this arti-cle at NEJM.org.

From the Division of Outcomes and Effec-tiveness Research, Department of Pub-lic Health, Weill Cornell Medical College, New York.

1. Casalino LP, Elster A, Eisenberg A, Lewis E, Montgomery J, Ramos D. Will pay-for-performance and quality reporting affect health care disparities? Health Aff (Millwood) 2007;26(3):w405-w414.2. Gaskin DJ, Spencer CS, Richard P, Ander-son GF, Powe NR, Laveist TA. Do hospitals provide lower-quality care to minorities than to whites? Health Aff (Millwood) 2008;27: 518-27.3. Jha AK, Orav EJ, Epstein AM. The effect of financial incentives on hospitals that serve poor patients. Ann Intern Med 2010;153:299-306.4. Werner RM, Dudley RA. Medicares new hospital value-based purchasing program is likely to have only a small impact on hospital payments. Health Aff (Millwood) 2012;31: 1932-40.5. Joynt KE, Jha AK. Characteristics of hospi-tals receiving penalties under the Hospital Readmissions Reduction Program. JAMA 2013;309:342-3.

DOI: 10.1056/NEJMp1312654Copyright 2013 Massachusetts Medical Society.

Will Value-Based Purchasing Increase Disparities?

Preserving Antibiotics, RationallyAidan Hollis, Ph.D., and Ziana Ahmed, B.A.Sc.

Antimicrobial resistance is a critical threat to public health. The value of antibiotics for hu-man health is immeasurable, but were one to try to measure, a plausible estimate of the increase in life expectancy attributable to antibiotics might be 2 to 10 years.1 If we multiply this in-crease by 300 million Americans and a dollar value of, say, $100,000 per life-year, we arrive at an estimate for the worth of the current stock of antibiotics of $60 trillion to $300 trillion in the United States alone. Unfor-tunately, this stock is being gradually depleted owing to ge-netic mutations in bacteria and the selective pressure caused by

the f lood of antibiotics released into the environment. A total of 51 tons of antibiotics are con-sumed daily in the United States alone, so the selective pressure in favor of resistant pathogens is strong.

The main use of this invalu-able resource is rather disappoint-ing: approximately 80% of anti-biotics in the United States are consumed in agriculture and aqua-culture (see pie chart). Antibiot-ics are fed to pigs to speed up growth and increase the efficiency of their digestion (see photo), add-ed to food pellets and dropped to salmon in cages in the seas, sprayed on fruit trees, and even embedded in marine paint to in-

hibit the formation of barnacles. Such promiscuous use of antibiot-ics is not surprising: nonphar-maceutical-grade antibiotics are typically priced at approximately $25 per kilogram, and there is little regulation or oversight of their use.

There is a great deal of con-cern that this profligate distribu-tion of antibiotics around the world is contributing to the de-velopment and spread of resis-tant organisms. Agricultural in-dustry groups, in line with their short-term financial interests, ar-gue that there is no conclusive proof that the antibiotics used in agriculture harm human health. Unfortunately, evidence is mount-

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Preserving Antibiotics, Rationally

ing that resistant pathogens are emerging and being selected for at least partly because of nonhu-man uses of antibiotics.2 Bacteria are not particular about whether they colonize a milk cow or a human, and they easily exchange genes conferring resistance. Much of the nonhuman use occurs at subtherapeutic levels that are nonetheless high enough to im-part an advantage to surviving bacteria, but so far there is a lack of evidence regarding the extent to which various uses contribute to resistance.

Recognizing the problem, the Food and Drug Administration banned the use of fluoroquino-lones in poultry in 2005. In 2012, it issued nonbinding guidance to farmers recommending that they avoid using antibiotics as animal-growth promoters, and in 2013, it encouraged pharmaceutical sup-pliers to voluntarily remove pro-duction uses from labeling with-in 3 years. In Europe, the use of antibiotics for growth promotion in animals has been banned, a move that has led to reductions in the volume of antibiotics used.In the Netherlands, the total vol-

ume of antibiotics sold initially remained unchanged, as farms reduced their use for growth promotion and increased their use for therapeutic purposes.3

Is a ban the right approach? There are many challenges. First, a ban would necessitate the mon-itoring of actual use, so that farmers who comply with the ban are not disadvantaged rela-tive to those who continue to use antibiotics. Requiring veterinary oversight would be problematic for geographically remote farms and fish farms and would neces-sitate a substantial increase in the number of veterinarians. More-over, defining exactly what is banned is like drawing a line on a slippery slope: it may not be clear whether an antibiotic is be-ing used for growth promotion, for prophylaxis to reduce the risk of infection in the face of stress-ful conditions, or both.

Second, the range of uses of antibiotics is wide, and their value varies substantially. In some ap-plications, an antibiotic may con-fer benefits worth slightly more than the cost of buying it; in oth-ers, a course of antibiotics may

save an animal or a whole herd of animals from death. If infection is predictable, pro-phylaxis may even reduce the to-tal use of antibiotics by eliminat-ing the need for therapeutic use. Barring all uses of a given type of antibiotic is inefficient; the goal should be to deter only the low-value applications.

Since it would impose costs on farmers, a ban would increase food prices. A ban on the use of antibiotics as animal-growth pro-moters would raise production costs in the United States by an estimated $1.2 billion to $2.5 bil-lion annually.4 Although this cost increase pales in comparison with the therapeutic value of antibiot-ics in humans, it would be felt disproportionately by poor Amer-icans and by farming operations that use animal-confinement sys-tems and rely on antibiotics.

An economically rational solu-tion is to impose a user fee on the nonhuman use of antibiotics. Every use of antibiotics increases selective pressure, thus undermin-ing the value for other users. In effect, each antibiotic can have only a limited amount of use, so

Livestock13,540,000 kg

Crops70,000 kg

Aquaculture150,000 kg

Humans3,290,000 kg

Pets150,000 kg

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Estimated Annual Antibiotic Use in the United States.

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it is appropriate to charge a fee, just as logging companies pay stumpage fees and oil compa-nies pay royalties. (A perfect fee would be calibrated to the extent of antibiotic resistance caused by each use; a practical fee, which is what we propose, would be based on the volume of antibiotics used.)

A user fee would have four important advantages over a ban. First, it would be relatively easy to administer, since it could be imposed at the manufacturing or importing stage.

Second, a user fee would deter low-value uses of antibiotics. Farms with good substitutes for antibiotics for example, vac-cinations or improved animal-management practices would be discouraged from using anti-biotics by higher prices, whereas farms with a high incidence of infections would probably con-tinue to use antibiotics. The idea is to allow the farmer or veteri-narian to decide whether the anti-biotic confers enough benefits to make it worth the higher price, rather than relying on the intru-sive, indiscriminate hand of gov-ernment.

Third, user fees would generate revenues that could help to pay for rewards to companies that suc-cessfully develop new antibiot-ics,5 or to subsidize antibiotic- research investments, or to support antimicrobial stewardship and

education programs. In effect, a user fee could help to restock and maintain the antibiotic cup-board, which is looking increas-ingly bare.

The benefits to human health would be substantial. By reduc-ing the volume of antibiotics, a user fee would mitigate the pres-sure of selection and diminish the prevalence of resistant patho-gens. In addition, it could sup-port the introduction of new drugs. According to our calcula-tions above, a 1% reduction in the usefulness of existing antibi-otics could impose costs of $600 billion to $3 trillion in lost hu-man health. It is vital to protect this essential resource.

A user-fee policy would simi-larly help agricultural production. Farms, no less than hospitals, suffer because of antibiotic resis-tance. Individual farms would benefit from a reduction in use of antibiotics by other farms and from the introduction of new drugs able to treat resistant in-fections.

The fourth key benefit of the user-fee approach, as compared with a ban, is international repli-cability. Resistant bacteria do not respect national borders. Although the United States would benefit from imposing user fees on its own, an even better approach would be an international treaty to recognize the fragility of our

common antibiotic resources and to impose user fees to be col-lected by national governments. A treaty would level the playing field for agricultural producers while mitigating the disastrous overuse of antibiotics. Such a treaty would also have a chance of attaining international compli-ance, since governments would be motivated to collect the reve-nues. By contrast, a ban, which disadvantages local producers while providing no revenues to government, would be much less attractive to enforce.

Disclosure forms provided by the authors are available with the full text of this article at NEJM.org.

From the Department of Economics, Univer-sity of Calgary, Calgary, AB, Canada, and In-centives for Global Health, Washington, DC (A.H.); and the Department of Economics, University of Toronto, Toronto (Z.A.).

1. McDermott W, Rogers DE. Social ramifi-cations of control of microbial disease. Johns Hopkins Med J 1982;151:302-12.2. Harrison EM, Paterson GK, Holden MTG, et al. Whole genome sequencing identifies zoonotic transmission of MRSA isolates with the novel mecA homologue mecC. EMBO Mol Med 2013;5:509-15.3. Cogliani C, Goosens H, Greko C. Restrict-ing antimicrobial use in food animals: lessons from Europe. Microbe 2011;6:274-9.4. National Research Council. The use of drugs in food animals: benefits and risks. Washington, DC: National Academy Press, 1999.5. Outterson K, Pogge T, Hollis A. Combat-ing antibiotic resistance through the Health Impact Fund. In: Cohen G, ed. The globaliza-tion of health care. Oxford, United Kingdom: Oxford University Press, 2013.

DOI: 10.1056/NEJMp1311479Copyright 2013 Massachusetts Medical Society.

Preserving Antibiotics, Rationally

Elder Self-Neglect How Can a Physician Help?Alexander K. Smith, M.D., M.P.H., Bernard Lo, M.D., and Louise Aronson, M.D.

Mr. L. is a 96-year-old widower with critical aortic stenosis and mild cognitive impairment who had become increasingly short of breath and exhausted

over the course of several weeks and needed 3 hours to get dressed on the day of admission. A con-cerned neighbor brought him to the hospital. He is not a candi-

date for aortic-valve replacement owing to poor functional status and coexisting conditions, and after several days of gentle diure-sis, he can barely walk across



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